Protein lipoxidation: Detection strategies and challenges

Redox Biology

Volumn 5, Issue , 2015, Pages 253-266

  Aldini, Giancarlo ^a   Domingues, M Rosário ^b   Spickett, Corinne M ^c   Domingues, Pedro ^b   Altomare, Alessandra ^a   Sánchez Gómez, Francisco J ^d   Oeste, Clara L ^d   Pérez Sala, Dolores ^d  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF AVEIRO   (Portugal)

^c ASTON UNIVERSITY   (United Kingdom)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Cyclopentenone prostaglandins; Electrophilic lipids; Mass spectrometry; Reactive carbonyl species; Target validation; Vimentin cysteine lipoxidation

Indexed keywords

4 HYDROXYNONENAL; ACROLEIN; ALDEHYDE; CARBONYL DERIVATIVE; CYCLOPENTENONE PROSTAGLANDIN; ELECTROPHILIC LIPID; LIPID; MALONALDEHYDE; PROSTAGLANDIN; RAS PROTEIN; REACTIVE CARBONYL SPECIES; UNCLASSIFIED DRUG; VIMENTIN; DINITROPHENYLHYDRAZINE; HYDRAZINE DERIVATIVE; LIPOPEPTIDE; PROTEIN;

BIOACCUMULATION; CHEMICAL INTERACTION; CHEMICAL LABELING; CLICK CHEMISTRY; COLLISIONAL INDUCED DISSOCIATION; DEGENERATIVE DISEASE; DISSOCIATION; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; LIPID METABOLISM; LIPID PEROXIDATION; LIPOXIDATION ADDUCT; MASS FRAGMENTOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METABOLIC LABELING; MOLECULAR DYNAMICS; MOLECULAR STABILITY; NONHUMAN; OXIDATION REDUCTION STATE; PATHOPHYSIOLOGY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN LIPOXIDATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEOMICS; REVIEW; STRUCTURE ACTIVITY RELATION; TANDEM MASS SPECTROMETRY; VALIDATION PROCESS; CHEMISTRY; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM;

ALDEHYDES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HYDRAZINES; LIPIDS; LIPOPEPTIDES; PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84930934147     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2015.05.003     Document Type: Review

References (114)

1. Vistoli G., De Maddis D., Cipak A., Zarkovic N., Carini M., Aldini G. Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radical Research 2013, 47:3-27. http://www.ncbi.nlm.nih.gov/pubmed/23767955, 10.3109/10715762.2013.815348.
2. Pamplona R. Advanced lipoxidation end-products. Chemico-Biological Interactions 2011, 192(1-2):14-20. http://www.ncbi.nlm.nih.gov/pubmed/21238437, 10.1016/j.cbi.2011.01.007.
3. Domingues R.M., Domingues P., Melo T., Pérez-Sala D., Reis A., Spickett C.M. Lipoxidation adducts with peptides and proteins: deleterious modifications or signaling mechanisms?. Journal of Proteomics 2013, 92:110-131. http://www.ncbi.nlm.nih.gov/pubmed/23770299, 10.1016/j.jprot.2013.06.004.
4. Vasil'ev Y.V., Tzeng S.C., Huang L., Maier C.S. Protein modifications by electrophilic lipoxidation products: adduct formation, chemical strategies and tandem mass spectrometry for their detection and identification. Mass Spectrometry Reviews 2014, 33(3):157-182. http://www.ncbi.nlm.nih.gov/pubmed/24818247, 10.1002/mas.21389.
5. Ullery J.C., Marnett L.J. Protein modification by oxidized phospholipids and hydrolytically released lipid electrophiles: investigating cellular responses. Biochimica Biophysica Acta 2012, 1818(10):2424-2435., 10.1016/j.bbamem.2012.04.014 22562025.
6. Stemmer U., Hermetter A. Protein modification by aldehydophospholipids and its functional consequences. Biochimica Biophysica Acta 2012, 1818(10):2436-2445. http://www.ncbi.nlm.nih.gov/pubmed/22450235, 10.1016/j.bbamem.2012.03.006.
7. Niki E. Lipid peroxidation: physiological levels and dual biological effects. Free Radical Biology and Medicine 2009, 47(5):469-484. http://www.ncbi.nlm.nih.gov/pubmed/19500666, 10.1016/j.freeradbiomed.2009.05.032.
8. Guéraud F., Atalay M., Bresgen N., Cipak A., Eckl P.M., Huc L., et al. Chemistry and biochemistry of lipid peroxidation products. Free Radical Research 2010, 44(10):1098-1124. http://www.ncbi.nlm.nih.gov/pubmed/20836659, 10.3109/10715762.2010.498477.
9. Reis A., Spickett C.M. Chemistry of phospholipid oxidation. Biochimica Biophysica Acta 2012, 1818(10):2374-2387. http://www.ncbi.nlm.nih.gov/pubmed/22342938, 10.1016/j.bbamem.2012.02.002.
10. Murphy S.A., Al-Aaswad N.M., Nicolaou A. Enzymatic oxidation of polyunsaturated fatty acids. Lipid Oxidation in Health and Disease 2015, CRC Press, London, UK. C.M. Spickett, H.J. Forman (Eds.).
11. Perry E.A., Castellani R.J., Moreira P.I., Nunomura A., Lui Q., Harris P.L., et al. Neurofilaments are the major neuronal target of hydroxynonenal-mediated protein cross-links. Free Radical Research 2013, 47(6-7):507-510. http://www.ncbi.nlm.nih.gov/pubmed/23566300, 10.3109/10715762.2013.794265.
12. Roberts L.J., Morrow J.D. Products of the isoprostane pathway: unique bioactive compounds and markers of lipid peroxidation. Cellular and Molecular Life Sciences 2002, 59(5):808-820. http://www.ncbi.nlm.nih.gov/pubmed/12088281, 10.1007/s00018-002-8469-8.
13. Sánchez-Gómez F.J., Díez-Dacal B., Pajares M.A., Llorca O., Pérez-Sala D. Cyclopentenone prostaglandins with dienone structure promote cross-linking of the chemoresistance-inducing enzyme glutathione transferase P1-1. Molecular Pharmacology 2010, 78(4):723-733. http://www.ncbi.nlm.nih.gov/pubmed/20631055, 10.1124/mol.110.065391.
14. Baraibar M.A., Friguet B. Oxidative proteome modifications target specific cellular pathways during oxidative stress, cellular senescence and aging. Experimental Gerontology 2013, 48(7):620-625. http://www.ncbi.nlm.nih.gov/pubmed/23127722, 10.1016/j.exger.2012.10.007.
15. Thomas J.P., Maiorino M., Ursini F., Girotti A.W. Protective action of phospholipid hydroperoxide glutathione peroxidase against membrane-damaging lipid peroxidation. in situ reduction of phospholipid and cholesterol hydroperoxides. Journal of Biological Chemistry 1990, 265(1):454-461. http://www.ncbi.nlm.nih.gov/pubmed/2294113.
16. Alary J., Guéraud F., Cravedi J.P. Fate of 4-hydroxynonenal in vivo: disposition and metabolic pathways. Molecular Aspects of Medicine 2003, 24(4-5):177-187. http://www.ncbi.nlm.nih.gov/pubmed/12892995, 10.1016/S0098-2997(03)00012-8.
17. Spite M., Baba S.P., Ahmed Y., Barski O.A., Nijhawan K., Petrash J.M., et al. Substrate specificity and catalytic efficiency of aldo-keto reductases with phospholipid aldehydes. Biochemical Journal 2007, 405(1):95-105. http://www.ncbi.nlm.nih.gov/pubmed/17381426, 10.1042/BJ20061743.
18. Ahmed E.K., Rogowska-Wrzesinska A., Roepstorff P., Bulteau A.L., Friguet B. Protein modification and replicative senescence of WI-38 human embryonic fibroblasts. Aging Cell 2010, 9(2):252-272. http://www.ncbi.nlm.nih.gov/pubmed/20102351, 10.1111/j.1474-9726.2010.00555.x.
19. Garzón B., Oeste C.L., Díez-Dacal B., Pérez-Sala D. Proteomic studies on protein modification by cyclopentenone prostaglandins: expanding our view on electrophile actions. Journal of Proteomics 2011, 74(11):2243-2263. http://www.ncbi.nlm.nih.gov/pubmed/21459170, 10.1016/j.jprot.2011.03.028.
20. Aldini G., Vistoli G., Regazzoni L., Gamberoni L., Facino R.M., Yamaguchi S., et al. Albumin is the main nucleophilic target of human plasma: a protective role against pro-atherogenic electrophilic reactive carbonyl species?. Chemical Research in Toxicology 2008, 21(4):824-835. http://www.ncbi.nlm.nih.gov/pubmed/18324789, 10.1021/tx700349r.
21. Jacobs A.T., Marnett L.J. Systems analysis of protein modification and cellular responses induced by electrophile stress. Accounts of Chemical Research 2010, 43(5):673-683. http://www.ncbi.nlm.nih.gov/pubmed/20218676, 10.1021/ar900286y.
22. Fang X., Fu Y., Long M.J., Haegele J.A., Ge E.J., Parvez S., et al. Temporally controlled targeting of 4-hydroxynonenal to specific proteins in living cells. Journal of the American Chemical Society 2013, 135(39):14496-14499. http://www.ncbi.nlm.nih.gov/pubmed/24015839, 10.1021/ja405400k.
23. Aldini G., Dalle-Donne I., Vistoli G., Maffei Facino R., Carini M. Covalent modification of actin by 4-hydroxy-trans-2-nonenal (HNE): LC-ESI-MS/MS evidence for Cys374 Michael adduction. Journal of Mass Spectrometry 2005, 40(7):946-954. http://www.ncbi.nlm.nih.gov/pubmed/15934040, 10.1002/jms.872.
24. Gayarre J., Sánchez D., Sánchez-Gómez F.J., Terrón M.C., Llorca O., Pérez-Sala D. Addition of electrophilic lipids to actin alters filament structure. Biochemical and Biophysical Research Communications 2006, 349(4):1387-1393. http://www.ncbi.nlm.nih.gov/pubmed/16979589, 10.1016/j.bbrc.2006.09.005.
25. Aldini G., Carini M., Vistoli G., Shibata T., Kusano Y., Gamberoni L., et al. Identification of actin as a 15-deoxy-Delta12,14-prostaglandin J2 target in neuroblastoma cells: mass spectrometric, computational, and functional approaches to investigate the effect on cytoskeletal derangement. Biochemistry 2007, 46(10):2707-2718. http://www.ncbi.nlm.nih.gov/pubmed/17297918, 10.1021/bi0618565.
26. Stamatakis K., Sánchez-Gómez F.J., Pérez-Sala D. Identification of novel protein targets for modification by 15-deoxy-Delta12,14-prostaglandin J2 in mesangial cells reveals multiple interactions with the cytoskeleton. Journal of the American Society Nephrology 2006, 17(1):89-98. http://www.ncbi.nlm.nih.gov/pubmed/16291835, 10.1681/ASN.2005030329.
27. Chavez J., Chung W.G., Miranda C.L., Singhal M., Stevens J.F., Maier C.S. Site-specific protein adducts of 4-hydroxy-2(E)-nonenal in human THP-1 monocytic cells: protein carbonylation is diminished by ascorbic acid. Chemical Research in Toxicology 2010, 23(1):37-47. http://www.ncbi.nlm.nih.gov/pubmed/20043646, 10.1021/tx9002462.
28. Aldini G., Granata P., Orioli M., Santaniello E., Carini M. Detoxification of 4-hydroxynonenal (HNE) in keratinocytes: characterization of conjugated metabolites by liquid chromatography/electrospray ionization tandem mass spectrometry. Journal of Mass Spectrometry 2003, 38(11):1160-1168. http://www.ncbi.nlm.nih.gov/pubmed/14648823, 10.1002/jms.533.
29. Yang J., Tallman K.A., Porter N.A., Liebler D.C. Quantitative chemoproteomics for site-specific analysis of protein alkylation by 4-hydroxy-2-nonenal in cells. Analytical Chemistry 2015, 87(5):2535-2541. http://www.ncbi.nlm.nih.gov/pubmed/25654326, 10.1021/ac504685y.
30. Butterfield D.A., Reed T., Sultana R. Roles of 3-nitrotyrosine- and 4-hydroxynonenal-modified brain proteins in the progression and pathogenesis of Alzheimer's disease. Free Radical Research 2011, 45(1):59-72. http://www.ncbi.nlm.nih.gov/pubmed/20942567, 10.3109/10715762.2010.520014.
31. Leonarduzzi G., Chiarpotto E., Biasi F., Poli G. 4-hydroxynonenal and cholesterol oxidation products in atherosclerosis. Molecular Nutrition and Food Research 2005, 49(11):1044-1049. http://www.ncbi.nlm.nih.gov/pubmed/16270277, 10.1002/mnfr.200500090.
32. Aldini G., Orioli M., Carini M. Protein modification by acrolein: relevance to pathological conditions and inhibition by aldehyde sequestering agents. Molecular Nutrition and Food Research 2011, 55(9):1301-1319. http://www.ncbi.nlm.nih.gov/pubmed/21805620, 10.1002/mnfr.201100182.
33. Dunér P., Gonçalves I., Grufman H., Edsfeldt A., To F., Nitulescu M., et al. Increased aldehyde-modification of collagen type IV in symptomatic plaques - a possible cause of endothelial dysfunction. Atherosclerosis 2015, 240(1):26-32. http://www.ncbi.nlm.nih.gov/pubmed/25746374, 10.1016/j.atherosclerosis.2015.02.043.
34. Tsimikas S., Witztum J.L. The role of oxidized phospholipids in mediating lipoprotein(a) atherogenicity. Current Opinion in Lipidology 2008, 19(4):369-377. http://www.ncbi.nlm.nih.gov/pubmed/18607184, 10.1097/MOL.0b013e328308b622.
35. Zhang W., Salomon R.G. Oxidized phospholipids, isolevuglandins, and atherosclerosis. Molecular Nutrition and Food Research 2005, 49(11):1050-1062. http://www.ncbi.nlm.nih.gov/pubmed/16270278, 10.1002/mnfr.200500056.
36. Taleb A., Witztum J.L., Tsimikas S. Oxidized phospholipids on apoB-100-containing lipoproteins: a biomarker predicting cardiovascular disease and cardiovascular events. Biomarkers in Medicine 2011, 5(5):673-694. http://www.ncbi.nlm.nih.gov/pubmed/22003918, 10.2217/bmm.11.60.
37. Mali V.R., Ning R., Chen J., Yang X.P., Xu J., Palaniyandi S.S. Impairment of aldehyde dehydrogenase-2 by 4-hydroxy-2-nonenal adduct formation and cardiomyocyte hypertrophy in mice fed a high-fat diet and injected with low-dose streptozotocin. Experimental Biology and Medicine 2014, 239(5):610-618. http://www.ncbi.nlm.nih.gov/pubmed/24651616, 10.1177/1535370213520109.
38. D'Souza A., Kurien B.T., Rodgers R., Shenoi J., Kurono S., Matsumoto H., et al. Detection of catalase as a major protein target of the lipid peroxidation product 4-HNE and the lack of its genetic association as a risk factor in SLE. BMC Medical Genetics 2008, 9:62. http://www.ncbi.nlm.nih.gov/pubmed/18606005, 10.1186/1471-2350-9-62.
39. Carbone D.L., Doorn J.A., Kiebler Z., Petersen D.R. Cysteine modification by lipid peroxidation products inhibits protein disulfide isomerase. Chemical Research in Toxicology 2005, 18(8):1324-1331. http://www.ncbi.nlm.nih.gov/pubmed/16097806, 10.1021/tx050078z.
40. Shearn C.T., Backos D.S., Orlicky D.J., Smathers-McCullough R.L., Petersen D.R. Identification of 5' AMP-activated kinase as a target of reactive aldehydes during chronic ingestion of high concentrations of ethanol. Journal ofBiological Chemistry 2014, 289(22):15449-15462. http://www.ncbi.nlm.nih.gov/pubmed/24722988, 10.1074/jbc.M113.543942.
41. Pradeep A.R., Agarwal E., Bajaj P., Rao N.S. 4-hydroxy-2-nonenal, an oxidative stress marker in crevicular fluid and serum in type 2 diabetes with chronic periodontitis. Contemporary Clinical Dentistry 2013, 4(3):281-285. http://www.ncbi.nlm.nih.gov/pubmed/24124291, 10.4103/0976-237X.118342.
42. Lee S.E., Park Y.S. Role of lipid peroxidation-derived alpha, beta-unsaturated aldehydes in vascular dysfunction. Oxidative Medicine and Cell Longevity 2013, 2013:629028.
43. Barrera G., Pizzimenti S., Ciamporcero E.S., Daga M., Ullio C., Arcaro A., et al. Role of 4-hydroxynonenal-protein adducts in human diseases. Antioxidants and Redox Signaling 2015, in press. 10.1089/ars.2014.6166.
44. McDowell R.E., McGeown J.G., Stitt A.W., Curtis T.M. Therapeutic potential of targeting lipid aldehydes and lipoxidation end-products in the treatment of ocular disease. Future Medicinal Chemistry 2013, 5(2):189-211. http://www.ncbi.nlm.nih.gov/pubmed/23360143, 10.4155/fmc.12.202.
45. Chen M., Curtis T.M., Stitt A.W. Advanced glycation end products and diabetic retinopathy. Current Medicinal Chemistry 2013, 20(26):3234-3240. http://www.ncbi.nlm.nih.gov/pubmed/23745547, 10.2174/09298673113209990025.
46. Madian A.G., Regnier F.E. Proteomic identification of carbonylated proteins and their oxidation sites. Journal of Proteome Research 2010, 9(8):3766-3780. http://www.ncbi.nlm.nih.gov/pubmed/20521848, 10.1021/pr1002609.
47. Mendez D., Hernaez M.L., Diez A., Puyet A., Bautista J.M. Combined proteomic approaches for the identification of specific amino acid residues modified by 4-hydroxy-2-nonenal under physiological conditions. Journal of Proteome Research 2010, 9(11):5770-5781. http://www.ncbi.nlm.nih.gov/pubmed/20818828, 10.1021/pr100555v.
48. Chavez J.D., Wu J., Bisson W., Maier C.S. Site-specific proteomic analysis of lipoxidation adducts in cardiac mitochondria reveals chemical diversity of 2-alkenal adduction. Journal of Proteomics 2011, 74(11):2417-2429. http://www.ncbi.nlm.nih.gov/pubmed/21513823, 10.1016/j.jprot.2011.03.031.
49. Charles R.L., Burgoyne J.R., Mayr M., Weldon S.M., Hubner N., Dong H., et al. Redox regulation of soluble epoxide hydrolase by 15-deoxy-delta-prostaglandin J2 controls coronary hypoxic vasodilation. Circulation Research 2011, 108(3):324-334. http://www.ncbi.nlm.nih.gov/pubmed/21164107, 10.1161/CIRCRESAHA.110.235879.
50. Díez-Dacal B., Pérez-Sala D. Anti-inflammatory prostanoids: focus on the interactions between electrophile signalling and resolution of inflammation. Scientific World Journal 2010, 10:655-675., 10.1100/tsw.2010.69 20419278.
51. Martínez A.E., Sánchez-Gómez F.J., Díez-Dacal B., Oeste C.L., Pérez-Sala D. 15-Deoxy-δ(12,14)-prostaglandin J2 exerts pro- and anti-inflammatory effects in mesangial cells in a concentration-dependent manner. Inflammation and Allergy Drug Targets 2012, 11(1):58-65., 10.2174/187152812798889349 22309084.
52. Renedo M., Gayarre J., García-Domínguez C.A., Pérez-Rodríguez A., Prieto A., Cañada F.J., et al. Modification and activation of Ras proteins by electrophilic prostanoids with different structure are site-selective. Biochemistry 2007, 46(22):6607-6616. http://www.ncbi.nlm.nih.gov/pubmed/17489560, 10.1021/bi602389p.
53. Oeste C.L., Díez-Dacal B., Bray F., García de Lacoba M., de la Torre B.G., Andreu D., et al. The C-terminus of H-Ras as a target for the covalent binding of reactive compounds modulating Ras-dependent pathways. PLOS One 2011, 6(1):e15866. http://www.ncbi.nlm.nih.gov/pubmed/21253588, 10.1371/journal.pone.0015866.
54. Cordis G.A., Das D.K., Riedel W. High-performance liquid chromatographic peak identification of 2,4-dinitrophenylhydrazine derivatives of lipid peroxidation aldehydes by photodiode array detection. Journal of Chromatography A 1998, 798(1-2):117-123. http://www.ncbi.nlm.nih.gov/pubmed/9542133, 10.1016/S0021-9673(97)01161-8.
55. Mateos R., Lecumberri E., Ramos S., Goya L., Bravo L. Determination of malondialdehyde (MDA) by high-performance liquid chromatography in serum and liver as a biomarker for oxidative stress. application to a rat model for hypercholesterolemia and evaluation of the effect of diets rich in phenolic antioxidants from fruits. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Science 2005, 827(1):76-82. http://www.ncbi.nlm.nih.gov/pubmed/16009604, 10.1016/j.jchromb.2005.06.035.
56. Zhu H., Li X., Shoemaker C.F., Wang S.C. Ultrahigh performance liquid chromatography analysis of volatile carbonyl compounds in virgin olive oils. Journal of Agricultural and Food Chemistry 2013, 61(50):12253-12259. http://www.ncbi.nlm.nih.gov/pubmed/24279346, 10.1021/jf404368m.
57. Siegel D., Meinema A.C., Permentier H., Hopfgartner G., Bischoff R. Integrated quantification and identification of aldehydes and ketones in biological samples. Analytical Chemistry 2014, 86(10):5089-5100. http://www.ncbi.nlm.nih.gov/pubmed/24745975, 10.1021/ac500810r.
58. Wang M., Fang H., Han X. Shotgun lipidomics analysis of 4-hydroxyalkenal species directly from lipid extracts after one-step in situ derivatization. Analytical Chemistry 2012, 84(10):4580-4586. http://www.ncbi.nlm.nih.gov/pubmed/22500579, 10.1021/ac300695p.
59. Milic I., Hoffmann R., Fedorova M. Simultaneous detection of low and high molecular weight carbonylated compounds derived from lipid peroxidation by electrospray ionization-tandem mass spectrometry. Analytical Chemistry 2013, 85(1):156-162. http://www.ncbi.nlm.nih.gov/pubmed/23186270, 10.1021/ac302356z.
60. Ni Z., Milic I., Fedorova M. Identification of carbonylated lipids from different phospholipid classes by shotgun and LC-MS lipidomics. Analytical and Bioanalytical Chemistry 2015, 25701423, in press.
61. Tomono S., Miyoshi N., Ohshima H. Comprehensive analysis of the lipophilic reactive carbonyls present in biological specimens by LC/ESI-MS/MS. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences 2015, 988:149-156. http://www.ncbi.nlm.nih.gov/pubmed/25777478, 10.1016/j.jchromb.2015.02.036.
62. García-Gómez D., Martínez-Lozano Sinues P., Barrios-Collado C., Vidal-de-Miguel G., Gaugg M., Zenobi R. Identification of 2-alkenals, 4-hydroxy-2-alkenals, and 4-hydroxy-2,6-alkadienals in exhaled breath condensate by UHPLC-HRMS and in breath by real-Time HRMS. Analytical Chemistry 2015, 87(5):3087-3093. http://www.ncbi.nlm.nih.gov/pubmed/25646646, 10.1021/ac504796p.
63. El-Maghrabey M.H., Kishikawa N., Ohyama K., Kuroda N. Analytical method for lipoperoxidation relevant reactive aldehydes in human sera by high-performance liquid chromatography-fluorescence detection. Analytical Biochemistry 2014, 464:36-42. http://www.ncbi.nlm.nih.gov/pubmed/25017470, 10.1016/j.ab.2014.07.002.
64. Ali M.F., Kishikawa N., Ohyama K., Mohamed H.A., Abdel-Wadood H.M., Mahmoud A.M., et al. Chromatographic determination of low-molecular mass unsaturated aliphatic aldehydes with peroxyoxalate chemiluminescence detection after fluorescence labeling with 4-(N,N-dimethylaminosulfonyl)-7-hydrazino-2,1,3-benzoxadiazole. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences 2014, 953-954:147-152. http://www.ncbi.nlm.nih.gov/pubmed/24614624, 10.1016/j.jchromb.2014.02.009.
65. Cui T., Schopfer F.J., Zhang J., Chen K., Ichikawa T., Baker P.R., et al. Nitrated fatty acids: endogenous anti-inflammatory signaling mediators. Journal of Biological Chemistry 2006, 281(47):35686-35698. http://www.ncbi.nlm.nih.gov/pubmed/16887803, 10.1074/jbc.M603357200.
66. Colzani M., Aldini G., Carini M. Mass spectrometric approaches for the identification and quantification of reactive carbonyl species protein adducts. Journal of Proteomics 2013, 92:28-50. http://www.ncbi.nlm.nih.gov/pubmed/23597925, 10.1016/j.jprot.2013.03.030.
67. Zhao J., Chen J., Zhu H., Xiong Y.L. Mass spectrometric evidence of malonaldehyde and 4-hydroxynonenal adductions to radical-scavenging soy peptides. Journal of Agricultural and Food Chemistry 2012, 60(38):9727-9736. http://www.ncbi.nlm.nih.gov/pubmed/22946674, 10.1021/jf3026277.
68. Gürbüz G., Heinonen M. LC-MS investigations on interactions between isolated beta-lactoglobulin peptides and lipid oxidation product malondialdehyde. Food Chemistry 2015, 175:300-305. http://www.ncbi.nlm.nih.gov/pubmed/25577084, 10.1016/j.foodchem.2014.11.154.
69. Steen H., Mann M. The ABC's (and XYZ's) of peptide sequencing. Nature Reviews Molecular Cell Biology 2004, 5(9):699-711. http://www.ncbi.nlm.nih.gov/pubmed/15340378, 10.1038/nrm1468.
70. Stevens S.M., Rauniyar N., Prokai L. Rapid characterization of covalent modifications to rat brain mitochondrial proteins after ex vivo exposure to 4-hydroxy-2-nonenal by liquid chromatography-tandem mass spectrometry using data-dependent and neutral loss-driven MS3 acquisition. Journal of Mass Spectrometry 2007, 42(12):1599-1605. http://www.ncbi.nlm.nih.gov/pubmed/18085542, 10.1002/jms.1349.
71. Rauniyar N., Stevens S.M., Prokai-Tatrai K., Prokai L. Characterization of 4-hydroxy-2-nonenal-modified peptides by liquid chromatography-tandem mass spectrometry using data-dependent acquisition: neutral loss-driven MS3 versus neutral loss-driven electron capture dissociation. Analytical Chemistry 2009, 81(2):782-789. http://www.ncbi.nlm.nih.gov/pubmed/19072288, 10.1021/ac802015m.
72. Méndez D., Hernáez M.L., Kamali A.N., Diez A., Puyet A., Bautista J.M. Differential carbonylation of cytoskeletal proteins in blood group O erythrocytes: potential role in protection against severe malaria. Infection, Genetics and Evolution 2012, 12(8):1780-1787. http://www.ncbi.nlm.nih.gov/pubmed/22771625, 10.1016/j.meegid.2012.06.013.
73. Fritz K.S., Kellersberger K.A., Gomez J.D., Petersen D.R. 4-HNE adduct stability characterized by collision-induced dissociation and electron transfer dissociation mass spectrometry. Chemical Research in Toxicology 2012, 25(4):965-970. http://www.ncbi.nlm.nih.gov/pubmed/22404378, 10.1021/tx300100w.
74. Carini M., Aldini G., Facino R.M. Mass spectrometry for detection of 4-hydroxy-trans-2-nonenal (HNE) adducts with peptides and proteins. Mass Spectrometry Reviews 2004, 23(4):281-305. http://www.ncbi.nlm.nih.gov/pubmed/15133838, 10.1002/mas.10076.
75. Spickett C.M., Reis A., Pitt A.R. Use of narrow mass-window, high-resolution extracted product ion chromatograms for the sensitive and selective identification of protein modifications. Analytical Chemistry 2013, 85(9):4621-4627. http://www.ncbi.nlm.nih.gov/pubmed/23534669, 10.1021/ac400131f.
76. Milic I., Melo T., Domingues M.R., Domingues P., Fedorova M. Heterogeneity of peptide adducts with carbonylated lipid peroxidation products. Journal of Mass Spectrometry 2015, 50(3):603-612. http://www.ncbi.nlm.nih.gov/pubmed/25800198, 10.1002/jms.3568.
77. Gao D., Willard B., Podrez E.A. Analysis of covalent modifications of proteins by oxidized phospholipids using a novel method of peptide enrichment. Analytical Chemistry 2014, 86(2):1254-1262. http://www.ncbi.nlm.nih.gov/pubmed/24350680, 10.1021/ac4035949.
78. Uchida K., Stadtman E.R. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. Journal of Biological Chemistry 1993, 268(9):6388-6393. http://www.ncbi.nlm.nih.gov/pubmed/8454610.
79. Golizeh M., Abusarah J., Benderdour M., Sleno L. Covalent binding of 4-hydroxynonenal to matrix metalloproteinase 13 studied by liquid chromatography-mass spectrometry. Chemical Research in Toxicology 2014, 27(9):1556-1565. http://www.ncbi.nlm.nih.gov/pubmed/25116078, 10.1021/tx5002095.
80. Smathers R.L., Fritz K.S., Galligan J.J., Shearn C.T., Reigan P., Marks M.J., et al. Characterization of 4-HNE modified L-FABP reveals alterations in structural and functional dynamics. PLOS One 2012, 7(6):e38459. http://www.ncbi.nlm.nih.gov/pubmed/22701647, 10.1371/journal.pone.0038459.
81. Anavi S., Ni Z., Tirosh O., Fedorova M. Steatosis-induced proteins adducts with lipid peroxidation products and nuclear electrophilic stress in hepatocytes. Redox Biology 2015, 4:158-168. http://www.ncbi.nlm.nih.gov/pubmed/25560244, 10.1016/j.redox.2014.12.009.
82. Rogowska-Wrzesinska A., Wojdyla K., Nedić O., Baron C.P., Griffiths H.R. Analysis of protein carbonylation -pitfalls and promise in commonly used methods. Free Radical Research 2014, 48(10):1145-1162. http://www.ncbi.nlm.nih.gov/pubmed/25072785, 10.3109/10715762.2014.944868.
83. Fedorova M., Bollineni R.C., Hoffmann R. Protein carbonylation as a major hallmark of oxidative damage: update of analytical strategies. Mass Spectrometry Reviews 2014, 33(2):79-97. http://www.ncbi.nlm.nih.gov/pubmed/23832618, 10.1002/mas.21381.
84. Dalle-Donne I., Carini M., Orioli M., Vistoli G., Regazzoni L., Colombo G., et al. Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radical Biology and Medicine 2009, 46(10):1411-1419. http://www.ncbi.nlm.nih.gov/pubmed/19268703, 10.1016/j.freeradbiomed.2009.02.024.
85. Bollineni R.C., Fedorova M., Hoffmann R. Qualitative and quantitative evaluation of derivatization reagents for different types of protein-bound carbonyl groups. Analyst 2013, 138(17):5081-5088. http://www.ncbi.nlm.nih.gov/pubmed/23833766, 10.1039/c3an00724c.
86. Bollineni R.C., Hoffmann R., Fedorova M. Proteome-wide profiling of carbonylated proteins and carbonylation sites in HeLa cells under mild oxidative stress conditions. Free Radical Biology and Medicine 2014, 68:186-195. http://www.ncbi.nlm.nih.gov/pubmed/24321318, 10.1016/j.freeradbiomed.2013.11.030.
87. Aluise C.D., Camarillo J.M., Shimozu Y., Galligan J.J., Rose K.L., Tallman K.A., et al. Site-specific, intramolecular cross-linking of Pin1 active Site residues by the lipid electrophile 4-oxo-2-nonenal. Chemical Research in Toxicology 2015, 28(4):817-827. http://www.ncbi.nlm.nih.gov/pubmed/25739016, 10.1021/acs.chemrestox.5b00038.
88. Fritz K.S., Galligan J.J., Smathers R.L., Roede J.R., Shearn C.T., Reigan P., et al. 4-hydroxynonenal inhibits SIRT3 via thiol-specific modification. Chemical Research in Toxicology 2011, 24(5):651-662. http://www.ncbi.nlm.nih.gov/pubmed/21449565, 10.1021/tx100355a.
89. Vunta H., Davis F., Palempalli U.D., Bhat D., Arner R.J., Thompson J.T., et al. The anti-inflammatory effects of selenium are mediated through 15-deoxy-delta12,14-prostaglandin J2 in macrophages. Journal of Biological Chemistry 2007, 282(25):17964-17973. http://www.ncbi.nlm.nih.gov/pubmed/17439952, 10.1074/jbc.M703075200.
90. Cernuda-Morollón E., Pineda-Molina E., Cañada F.J., Pérez-Sala D. 15-Deoxy-delta 12,14-prostaglandin J2 inhibition of NF-kappaB-DNA binding through covalent modification of the p50 subunit. Journal of Biological Chemistry 2001, 276(38):35530-35536. http://www.ncbi.nlm.nih.gov/pubmed/11466314, 10.1074/jbc.M104518200.
91. Takahashi N., Mizuno Y., Kozai D., Yamamoto S., Kiyonaka S., Shibata T., et al. Molecular characterization of TRPA1 channel activation by cysteine-reactive inflammatory mediators. Channels 2008, 2(4):287-298. http://www.ncbi.nlm.nih.gov/pubmed/18769139, 10.4161/chan.2.4.6745.
92. Artim D.E., Bazely F., Daugherty S.L., Sculptoreanu A., Koronowski K.B., Schopfer F.J., et al. Nitro-oleic acid targets transient receptor potential (TRP) channels in capsaicin sensitive afferent nerves of rat urinary bladder. Experimental Neurology 2011, 232(1):90-99. http://www.ncbi.nlm.nih.gov/pubmed/21867704, 10.1016/j.expneurol.2011.08.007.
93. 2 protein interactions and inhibition of cellular proliferation. Prostaglandins 1995, 50(5-6):359-375. http://www.ncbi.nlm.nih.gov/pubmed/8838245, 10.1016/0090-6980(95)00136-0.
94. 1 allows assessment of PPAR-independent effects and identification of novel cellular targets for covalent modification. Chemico-Biological Interactions 2010, 183(1):212-221. http://www.ncbi.nlm.nih.gov/pubmed/19800325, 10.1016/j.cbi.2009.09.019.
95. Higdon A.N., Dranka B.P., Hill B.G., Oh J.Y., Johnson M.S., Landar A., et al. Methods for imaging and detecting modification of proteins by reactive lipid species. Free Radical Biology and Medicine 2009, 47(3):201-212. http://www.ncbi.nlm.nih.gov/pubmed/19446632, 10.1016/j.freeradbiomed.2009.05.009.
96. Cummins T.D., Higdon A.N., Kramer P.A., Chacko B.K., Riggs D.W., Salabei J.K., Dell'Italia L.J., Zhang J., Darley-Usmar V.M., Hill B.G. Utilization of fluorescent probes for the quantification and identification of subcellular proteomes and biological processes regulated by lipid peroxidation products. Free Radical Biology and Medicine 2013, 59:56-68. http://www.ncbi.nlm.nih.gov/pubmed/22954622, 10.1016/j.freeradbiomed.2012.08.014.
97. Vila A., Tallman K.A., Jacobs A.T., Liebler D.C., Porter N.A., Marnett L.J. Identification of protein targets of 4-hydroxynonenal using click chemistry for ex vivo biotinylation of azido and alkynyl derivatives. Chemical Research in Toxicology 2008, 21(2):432-444. http://www.ncbi.nlm.nih.gov/pubmed/18232660, 10.1021/tx700347w.
98. Pérez-Sala D. Electrophilic eicosanoids: signaling and targets. Chemico-Biological Interactions 2011, 192(1-2):96-100. http://www.ncbi.nlm.nih.gov/pubmed/20970408, 10.1016/j.cbi.2010.10.003.
99. Gayarre J., Stamatakis K., Renedo M., Pérez-Sala D. Differential selectivity of protein modification by the cyclopentenone prostaglandins PGA1 and 15-deoxy-delta12,14-PGJ2: role of glutathione. FEBS Letters 2005, 579(25):5803-5808. http://www.ncbi.nlm.nih.gov/pubmed/16223487, 10.1016/j.febslet.2005.09.069.
100. Oeste C.L., Pérez-Sala D. Modification of cysteine residues by cyclopentenone prostaglandins: interplay with redox regulation of protein function. Mass Spectrometry Reviews 2014, 33(2):110-125. http://www.ncbi.nlm.nih.gov/pubmed/23818260, 10.1002/mas.21383.
101. Diers A.R., Higdon A.N., Ricart K.C., Johnson M.S., Agarwal A., Kalyanaraman B., et al. Mitochondrial targeting of the electrophilic lipid 15-deoxy-delta12,14-prostaglandin J2 increases apoptotic efficacy via redox cell signalling mechanisms. Biochemical Journal 2010, 426(1):31-41. http://www.ncbi.nlm.nih.gov/pubmed/19916962, 10.1042/BJ20091293.
102. Sánchez-Gómez F.J., Gayarre J., Avellano M.I., Pérez-Sala D. Direct evidence for the covalent modification of glutathione-S-transferase P1-1 by electrophilic prostaglandins: implications for enzyme inactivation and cell survival. Archives of Biochemistry and Biophysics 2007, 457(2):150-159. http://www.ncbi.nlm.nih.gov/pubmed/17169324, 10.1016/j.abb.2006.10.032.
103. Sánchez-Gómez F.J., Dorado C.G., Ayuso P., Agúndez J.A., Pajares M.A., Pérez-Sala D. Modulation of GSTP1-1 oligomerization by electrophilic inflammatory mediators and reactive drugs. Inflammation and Allergy Drug Targets 2013, 12(3):162-171., 10.2174/1871528111312030002 23596995.
104. Sánchez-Gómez F.J., Cernuda-Morollón E., Stamatakis K., Pérez-Sala D. Protein thiol modification by 15-deoxy-delta12,14-prostaglandin J2 addition in mesangial cells: role in the inhibition of pro-inflammatory genes. Molecular Pharmacology 2004, 66(5):1349-1358. http://www.ncbi.nlm.nih.gov/pubmed/15317873, 10.1124/mol.104.002824.
105. Baraibar M.A., Ladouce R., Friguet B. Proteomic quantification and identification of carbonylated proteins upon oxidative stress and during cellular aging. Journal of Proteomics 2013, 92:63-70. 10.1016/j.jprot.2013.05.008.
106. Uchida K., Szweda L.I., Chae H.Z., Stadtman E.R. Immunochemical detection of 4-hydroxynonenal protein adducts in oxidized hepatocytes. Proceedings of National Academy of Sciences of the United States of America 1993, 90(18):8742-8746. http://www.ncbi.nlm.nih.gov/pubmed/8378358, 10.1073/pnas.90.18.8742.
107. Shibata T., Kondo M., Osawa T., Shibata N., Kobayashi M., Uchida K. 15-deoxy-Delta 12,14-prostaglandin J2. A prostaglandin D2 metabolite generated during inflammatory processes. Journal of Biological Chemistry 2002, 277(12):10459-10466. http://www.ncbi.nlm.nih.gov/pubmed/11786541, 10.1074/jbc.M110314200.
108. Kato Y. The formation of lipid hydroperoxide-derived amide-type lysine adducts on proteins: a review of current knowledge. Subcellular Biochemistry 2014, 77:21-39. http://www.ncbi.nlm.nih.gov/pubmed/24374915, 10.1007/978-94-007-7920-4_2.
109. Shiraki T., Kamiya N., Shiki S., Kodama T.S., Kakizuka A., Jingami H. Alpha,beta-unsaturated ketone is a core moiety of natural ligands for covalent binding to peroxisome proliferator-activated receptor gamma. Journal of Biological Chemistry 2005, 280(14):14145-14153. http://www.ncbi.nlm.nih.gov/pubmed/15695504, 10.1074/jbc.M500901200.
110. Díez-Dacal B., Gayarre J., Gharbi S., Timms J.F., Coderch C., Gago F., et al. Identification of aldo-keto reductase AKR1B10 as a selective target for modification and inhibition by prostaglandin A(1): implications for antitumoral activity. Cancer Research 2011, 71(12):4161-4171. http://www.ncbi.nlm.nih.gov/pubmed/21507934, 10.1158/0008-5472.CAN-10-3816.
111. 1: focus on vimentin. Journal of Mass Spectrometry 2007, 42(11):1474-1484. http://www.ncbi.nlm.nih.gov/pubmed/17960581, 10.1002/jms.1291.
112. Kim H.J., Ha S., Lee H.Y., Lee K.J. Rosics: chemistry and proteomics of cysteine modifications in redox biology. Mass Spectrometry Reviews 2015, 34(2):184-208. http://www.ncbi.nlm.nih.gov/pubmed/24916017, 10.1002/mas.21430.
113. Pérez-Sala D., Oeste C.L., Martínez A.E., Garzón B., Carrasco M.J., Cañada F.J. Vimentin filament organization and stress sensing depend on its single cysteine residue and zinc binding. Nature Communications 2015, 6:7287., 10.1038/ncomms8287.
114. Tsapara A., Kardassis D., Moustakas A., Gravanis A., Stournaras C. Expression and characterization of Cys374 mutated human beta-actin in two different mammalian cell lines: impaired microfilament organization and stability. FEBS Letters 1999, 455(1-2):117-122. http://www.ncbi.nlm.nih.gov/pubmed/10428484, 10.1016/S0014-5793(99)00848-0.